Squid as Elite Athletes: Locomotory, Respiratory, and Circulatory Integration

Stella

2007

Journal of Morphology

148

118

The morphology of the musculature and connective tissues of the arms of Octopus bimaculoides was analyzed with light microscopy. We also studied O. briareus and O. digueti, which possess relatively more elongate and less elongate arms, respectively. The morphology of the arms was found to be remarkably uniform among species. The arms consist of a densely packed three-dimensional arrangement of muscle fibers and connective tissue fibers surrounding a central axial nerve cord. Three primary muscle fiber orientations were observed: 1) transverse muscle fibers oriented in planes perpendicular to the long axis of the arm; 2) longitudinal muscle fibers oriented parallel to the long axis; and 3) oblique muscle fibers arranged in helixes around the arm. The proportion of the arm cross section occupied by each of these muscle fiber groups (relative to the total cross sectional area of the musculature) remains constant along the length of the arm, even though the arm tapers from base to tip. A thin circular muscle layer wraps the arm musculature on the aboral side only. Much of this musculature has its origin and insertion on several robust connective tissue sheets including a layer surrounding the axial nerve cord and crossed-fiber connective tissue sheets located on the oral and the aboral sides of the arm. An additional thin layer of connective tissue wraps the arm musculature laterally and also serves as a site of origin and insertion of some of the muscle fibers. The fibers of the oral and aboral crossed-fiber connective tissue sheets are arranged oblique to the long axis of the arm with the same fiber angle as the oblique muscle layers that originate and insert on the sheets. The oblique muscle layers and the crossed-fiber connective tissue sheets thus form composite right- and left-handed helical fiber arrays. Analysis of arm morphology from the standpoint of biomechanics suggests that the transverse musculature is responsible for elongation of the arms, the longitudinal musculature is responsible for shortening, and the oblique muscle layers and associated connective tissues create torsion. Arm bending may involve unilateral contraction of longitudinal muscle bundles in combination with resistance to arm diameter increase due to contraction of the transverse musculature or passive stiffness of the arm tissues. The arms may also be bent by a combination of decrease in diameter due to contraction of the transverse musculature and maintenance of constant length on one side of the arm by unilateral activity of longitudinal muscle bundles. An increase in flexural stiffness of the arm may be achieved by cocontraction of the transverse and longitudinal muscle. Torsional stiffness may be increased by simultaneous contraction of both the right- and left-handed oblique muscle layers.

Section: Materials and Methods Experimental Animals Histologymentioning

confidence: 99%

The arrangement and function of octopus arm musculature and connective tissue

Stella

2007

Journal of Morphology

148

118

“…Four adult specimens of Octopus bimaculoides (70 -99 g wet weight), obtained from the National Resource Center for Cephalopods (Galveston, TX), were quickly and lightly anaesthetized using 2.5% ethanol in seawater (O'Dor et al, 1990). After the specimens were relaxed, the buccal masses were removed and placed in small bowls containing aerated seawater chilled to 17°C.…”

Section: Methodsmentioning

confidence: 99%

Functional morphology of the cephalopod buccal mass: A novel joint type

Uyeno

2005

J. Morphol.

The arrangement of the musculature and connective tissues of the buccal mass of the coleoid cephalopods Octopus bimaculoides, Sepia officinalis, and Loliguncula brevis was examined using dissection and histology. Serial sections in three mutually perpendicular planes were used to identify the muscles and connective tissues responsible for beak movements and stability and to describe their morphology and fiber trajectories. Four major beak muscles were identified: the anterior, posterior, superior, and lateral mandibular muscles. The anterior, posterior, and superior mandibular muscles connect the upper beak and the lower beak. Although the lateral mandibular muscles originate on the upper beak, they do not connect to the lower beak and instead insert on a connective tissue sheath surrounding the buccal mass. Examination of the fibers of the lateral mandibular muscles reveals that they have the organization of a muscular hydrostat, with muscle fibers oriented in three mutually perpendicular orientations. Although the beaks are capable of complex opening, closing, and shearing movements, they do not contact one another and are instead connected only by the musculature of the buccal mass. Based on the morphological analysis and observations of freshly dissected beaks undergoing the stereotyped bite cycle, the functional role of the beak muscles is hypothesized. The anterior and superior mandibular muscles are likely responsible for beak closing and shearing movements. The posterior mandibular muscle is likely also involved in beak closing, but may act synergistically with the lateral mandibular muscles to open the beaks. The lateral mandibular muscles may use a muscular-hydrostatic mechanism to control the location of the pivot between the beaks and to generate the force required for beak opening. The lack of contact between the beaks and the morphology of the lateral mandibular muscles suggests that the buccal mass of coleoid cephalopods may represent a previously unexamined flexible joint mechanism. The term "muscle articulation" is proposed here to denote the importance of the musculature in the function of such a joint.

“…Given the relatively small cross-sectional areas of these two muscles (Uyeno and Kier, 2005), the forces generated by the anterior and posterior mandibular muscles may be relatively lower than those generated by the superior and lateral mandibular muscles. were lightly anaesthetized using 2-3% ethanol in seawater for 2.5-7·min until arm activity ceased (O'Dor et al, 1990). After the specimen was relaxed, the brain was bisected, the interbuccal connectives were severed, and the buccal mass was removed and placed in a glass test chamber containing artificial seawater (NaCl, 470·mmol·l ; glucose, 20·mmol·l -1 ; Hepes, 10·mmol·l -1 ; adjusted to pH·7.8 with 2.0·mol·l -1 NaOH) (Milligan et al, 1997) chilled to 17°C.…”

Section: The Lateral Mandibular Musclesmentioning

confidence: 99%

Electromyography of the buccal musculature of octopus (Octopus bimaculoides): a test of the function of the muscle articulation in support and movement

Uyeno

Journal of Experimental Biology

2007

SUMMARY The buccal mass musculature of the octopus (Octopus bimaculoides)was studied with electromyography to test the predictions of a previous morphological study in which we suggested that the muscles of the buccal mass serve as both the effectors of movement and as the joint itself, forming a new category of flexible joint termed a `muscle articulation'. The predictions of muscle function were tested by correlating muscle electrical activity in isolated buccal masses with spontaneous beak movements. Bipolar electromyography electrodes were implanted in the various beak muscles and beak position was recorded simultaneously with an electronic movement monitor(N=14). The results are consistent with the hypothesis that the lateral mandibular muscles produce opening movements of the beaks and provide the first definitive explanation of the opening mechanism. The results are also consistent with the hypothesis that the superior mandibular muscle functions primarily in closing. Co-contraction of the lateral mandibular muscles and the superior mandibular muscles was also observed, suggesting that these muscles may also stabilize the beaks during movement or provide a means of controlling the location of the pivot between the beaks. This study provides an important first test of the predictions of the role of the complex musculature found in muscle articulations such as the cephalopod buccal mass.